Giant squids (Architeuthis dux) are the second largest cephalopods in the ocean, and their size is only exceeded by the colossal squid (Mesonychoteuthis hamiltoni). They can achieve 200 cm in mantle length [1]. It has been reported that giant squids live in the depth range of 300–1000 m [1–3], where the visual environment is extremely dim and almost without sunlight even during daytime [4]. Instead, the main light source at this depth is the bioluminescence from other organisms, such as the photophores on fish and other cephalopods [5,6]. Living in such a low light environment, giant squids have needed to develop a unique visual system that allows them effectively to find prey, predators and mates [7–11].

In addition to their large body, giant squids are also known for their enormous eyeballs [4,12]. A previous analysis of the Architeuthis eye suggested that the large diameters of the pupil and eye provide giant squids with a special advantage when detecting predators at far distance [13]. The retinal image from the eye in squid is sent to the optic lobe, a major brain area just behind the eyeball, where it undergoes visual information processing [14]. The optic lobe is a complex neural structure that is made up of the outer cortex, also called the deep retina [15], which contains visual analysing systems that process the input from the eye, and the central medulla, which is a higher motor centre responsible for controlling, for example, dynamic body patterns [14,16–18]. Despite there being significant knowledge of the giant eye in Architeuthis [13], the morphology and function of the optic lobe in giant squids has not been studied systematically. In this study, a rare sample of the optic lobe from a giant squid (A. dux, male, mantle length 89 cm; figure 1) was scanned using high-resolution magnetic resonance imaging (MRI) in order to visualize its general morphology and internal structure. The neural organization in the optic lobe was then quantified and compared with other cephalopod species. Figure 1.

The giant squid specimen. (a) The giant squid after fixation. Mantle length, 89 cm when measured freshly but 70 cm after fixation and dehydration; full length, approximately 4 m; scale bar, 50 cm. (b) A mature sperm mass (arrowhead) was evident beneath the penis (arrow). Scale bar, 1 cm. (c) The giant eye. The eyeball has dropped into the eye socket, thus only the lens (arrow) is visible. Scale bar, 5 cm.

Unlike typical squids, giant squids have a relatively small pair of optic lobes just behind their huge eyeballs; furthermore, there is an enlarged semi-annular tissue called the white body [21,22] that separates the eyeball and the optic lobe (figure 2a). The white body, a haematopoietic organ in cephalopods [23], is in contact with the dorsolateral side of the optic lobe and holds the eyeball in place. Numerous optic nerve fibres project from the retina directly into the lateral side of the optic lobe without passing through the white body (figure 2b, lateral view). The optic tract region, which is the main output site of the optic lobe, can be clearly seen on the medial side (figure 2b, medial view). The MRI scan of the optic lobe revealed for the first time that the giant squid has a relatively thicker cortex together with a less organized medulla (figure 2c; see also electronic supplementary material, Movie S1). Interestingly, the three-dimensional reconstruction of the optic lobe from the MRI scan showed that there is a prominent concave area on the ventrolateral side (figure 2d; see also electronic supplementary material, Movie S2). Figure 2.

The optic lobe of Architeuthis is relatively flat and concave ventrolaterally with a prominent white body that surrounds dorsolaterally. (a) A schematic drawing of the optic lobe, white body and eyeball relative to its head. (b) The photos of dissected optic lobe (arrow head) and white body (arrow). The eyeball was removed to reveal optic nerve bundles and concave structure at the ventrolateral side. The medial view shows the optic tract region (arrow). Scale bar, 1 cm. (c) Three slices of images from the MRI scan showing the internal structure of the optic lobe. The bright region shows the neuropil-rich zone and the dark region represents the aggregation of cell somata. The cortex can be readily distinguished from the medulla in the MRI scan (see electronic supplementary material, Movie S1). The ventral region of the optic lobe is much narrower than the dorsal region, which confirms a significant concaveness on the ventrolateral side. Scale bar, 1 cm. (d) A three-dimensional rendition of the MRI scan showing the shape of the optic lobe in both lateral and medial views (see electronic supplementary material, Movie S2). D, dorsal; A, anterior; L, lateral. Scale bar, 1 cm.

Living in deep sea with a pair of enormous eyeballs as part of its head, the brain of the giant squid is subjected to significant compression due to the two eyes. It has been reported that the white body is a haematopoietic organ, namely a site for haematocyte formation in coleoid cephalopods [21,23]. Although not related to its original function, in the giant squid, the unusually large white body surrounds the optic lobe dorsolaterally (figure 2a) and is likely to function as a cushion for the huge eyeball as well as a means of protecting the optic lobe [22]. As a consequence of the presence of the eyeball compression, the concaveness found on the ventrolateral side of the optic lobe in Architeuthis is much more prominent than in Sepioteuthis and Sepia (figure 3b). This is also consistent with the neural anatomy of Teuthida, where the distance of two eyes is closer than in Sepiida species [25], thus pressing the optic lobe laterally even more.

In addition to the highly compressed optic lobe in giant squids, there is a large mismatch in size between the eyeball and the optic lobe when these are compared with the other two cephalopod species (figure 3a). A previous anatomical study has also indicated that Architeuthis has the smallest ratio of the optic lobe to the rest of the whole brain among all cephalopods that have been examined [26]. This evidence suggests that the optic lobe is relatively less important in giant squids when compared with other lobes found in cephalopod brains. However, if the relative thickness of the cortex in the optic lobe of giant squids is compared with that of oval squids and cuttlefish, it was clear that the giant squid is not that different from oval squids, while being significantly thicker than in cuttlefish (figure 3c). This observation is largely consistent with an early histological study of the optic lobe of Architeuthis [22]. Furthermore, the fact that the intensity of the cortex in the giant squid is the lowest one among these three cephalopods (figure 3d) also suggests that the giant squid has relatively more cells in the cortex than the two shallow-water species of cephalopods examined. This implies that the size mismatch between the giant eye and the optic lobe in Architeuthis is likely to be a result of a much reduced medulla within the optic lobe.

The medulla of the optic lobe in cephalopods is a higher visuomotor centre that mainly controls the body patterns associated with various visual behaviours including camouflage and communication [18,27,28]. The finding that the giant squid has a relatively small medulla suggests that body pattern control is less complex in the Oegopsina, namely the giant squids and Humboldt squids, which are known to show simple flashing and flickering on their skins only [29]. This study thus provides the first evidence to support that giant squids with large eyes have well-developed visual processing systems within the optic lobe. Furthermore, these squids exhibit less demanding body patterning behaviours and have less well-developed visual communication and this is perhaps because they are deep-sea animals living in dim light from bioluminescence for most of their life cycle. The end result of this would seem to be an evolutionary drive towards disproportionally smaller optic lobes.